In response to touch, some carnivorous plants such as the Venus flytrap have evolved spectacular movements to capture animals for nutrient acquisition. However, the molecules that confer this ...sensitivity remain unknown. We used comparative transcriptomics to show that expression of three genes encoding homologs of the MscS-Like (MSL) and OSCA/TMEM63 family of mechanosensitive ion channels are localized to touch-sensitive trigger hairs of Venus flytrap. We focus here on the candidate with the most enriched expression in trigger hairs, the MSL homolog FLYCATCHER1 (FLYC1). We show that
transcripts are localized to mechanosensory cells within the trigger hair, transfecting
induces chloride-permeable stretch-activated currents in naïve cells, and transcripts coding for
homologs are expressed in touch-sensing cells of Cape sundew, a related carnivorous plant of the Droseraceae family. Our data suggest that the mechanism of prey recognition in carnivorous Droseraceae evolved by co-opting ancestral mechanosensitive ion channels to sense touch.
Plant architecture is optimized for the local light environment. In response to foliar shade or neighbor proximity (low red to far-red light), some plant species exhibit shade-avoiding phenotypes, ...including increased stem and hypocotyl growth, which increases the likelihood of outgrowing competitor plants. If shade persists, early flowering and the reallocation of growth resources to stem elongation ultimately affect the yield of harvestable tissues in crop species. Previous studies have shown that hypocotyl growth in low red to far-red shade is largely dependent on the photoreceptor phytochrome B and the phytohormone auxin. However, where shade is perceived in the plant and how auxin regulates growth spatially are less well understood. Using the oilseed and vegetable crop species Brassica rapa, we show that the perception of low red to far-red shade by the cotyledons triggers hypocotyl cell elongation and auxin target gene expression. Furthermore, we find that following shade perception, elevated auxin levels occur in a basipetal gradient away from the cotyledons and that this is coincident with a gradient of auxin target gene induction. These results show that cotyledon-generated auxin regulates hypocotyl elongation. In addition, we find in mature B. rapa plants that simulated shade does not affect seed oil composition but may affect seed yield. This suggests that in field settings where mutual shading between plants may occur, a balance between plant density and seed yield per plant needs to be achieved for maximum oil yield, while oil composition might remain constant.
Growth of a complex multicellular organism requires coordinated changes in diverse cell types. These cellular changes generate organs of the correct size, shape, and functionality. In plants, the ...growth hormone auxin induces stem elongation in response to shade; however, which cell types of the stem perceive the auxin signal and contribute to organ growth is poorly understood. Here, we blocked the transcriptional response to auxin within specific tissues to show that auxin signaling is required in many cell types for correct hypocotyl growth in shade, with a key role for the epidermis. Combining genetic manipulations in Arabidopsis thaliana with transcriptional profiling of the hypocotyl epidermis from Brassica rapa, we show that auxin acts in the epidermis in part by inducing activity of the locally acting, growth-promoting brassinosteroid pathway. Our findings clarify cell-specific auxin function in the hypocotyl and highlight the complexity of cell type interactions within a growing organ.
Neuronal receptive endings, such as dendritic spines and sensory protrusions, are structurally remodeled by experience. How receptive endings acquire their remodeled shapes is not well understood. In ...response to environmental stressors, the nematode Caenorhabditis elegans enters a diapause state, termed dauer, which is accompanied by remodeling of sensory neuron receptive endings. Here, we demonstrate that sensory receptive endings of the AWC neurons in dauers remodel in the confines of a compartment defined by the amphid sheath (AMsh) glial cell that envelops these endings. AMsh glia remodel concomitantly with and independently of AWC receptive endings to delimit AWC receptive ending growth. Remodeling of AMsh glia requires the OTD/OTX transcription factor TTX-1, the fusogen AFF-1 and probably the vascular endothelial growth factor (VEGFR)-related protein VER-1, all acting within the glial cell. ver-1 expression requires direct binding of TTX-1 to ver-1 regulatory sequences, and is induced in dauers and at high temperatures. Our results demonstrate that stimulus-induced changes in glial compartment size provide spatial constraints on neuronal receptive ending growth.
Like other complex multicellular organisms, plants are composed of different cell types with specialized shapes and functions. For example, most laminar leaves consist of multiple photosynthetic cell ...types. These cell types include the palisade mesophyll, which typically forms one or more cell layers on the adaxial side of the leaf. Despite their importance for photosynthesis, we know little about how palisade cells differ at the molecular level from other photosynthetic cell types. To this end, we have used a combination of cell-specific profiling using fluorescence-activated cell sorting and single-cell RNA-sequencing methods to generate a transcriptional blueprint of the palisade mesophyll in Arabidopsis thaliana leaves. We find that despite their unique morphology, palisade cells are otherwise transcriptionally similar to other photosynthetic cell types. Nevertheless, we show that some genes in the phenylpropanoid biosynthesis pathway have both palisade-enriched expression and are light-regulated. Phenylpropanoid gene activity in the palisade was required for production of the ultraviolet (UV)-B protectant sinapoylmalate, which may protect the palisade and/or other leaf cells against damaging UV light. These findings improve our understanding of how different photosynthetic cell types in the leaf can function uniquely to optimize leaf performance, despite their transcriptional similarities.
Animal nervous systems remodel following stress. Although global stress-dependent changes are well documented, contributions of individual neuron remodeling events to animal behavior modification are ...challenging to study. In response to environmental insults, C. elegans become stress-resistant dauers. Dauer entry induces amphid sensory organ remodeling in which bilateral AMsh glial cells expand and fuse, allowing embedded AWC chemosensory neurons to extend sensory receptive endings. We show that amphid remodeling correlates with accelerated dauer exit upon exposure to favorable conditions and identify a G protein-coupled receptor, REMO-1, driving AMsh glia fusion, AWC neuron remodeling, and dauer exit. REMO-1 is expressed in and localizes to AMsh glia tips, is dispensable for other remodeling events, and promotes stress-induced expression of the remodeling receptor tyrosine kinase VER-1. Our results demonstrate how single-neuron structural changes affect animal behavior, identify key glial roles in stress-induced nervous system plasticity, and demonstrate that remodeling primes animals to respond to favorable conditions.
Display omitted
•The glial GPCR REMO-1 regulates stress-induced neural plasticity in C. elegans•REMO-1 functions cell-autonomously to regulate glial and neuronal remodeling•REMO-1-dependent remodeling primes animals to respond to favorable conditions
Lee et al. provide molecular insight into how stress-induced sensory organ remodeling affects behavior in C. elegans. They identify a glial GPCR, REMO-1, that drives structural remodeling of sensory neurons and associated glia. This alteration of a single neuron-glia pair primes animals to respond efficiently to favorable environmental conditions.
This article comments on:
Pavlovič A, Koller J, Vrobel O, Chamrád I, Lenobel R, and Tarkowski P. 2024. Is the co-option of jasmonate signalling for botanical carnivory a universal trait for all ...carnivorous plants? Journal of Experimental Botany 75, 334–349.
Despite a growing number of descriptive studies that show Single-minded 2 (Sim2) is not only essential for murine survival, but also upregulated in colon, prostate and pancreatic tumours, there is a ...lack of direct target genes identified for this basic helix-loop-helix/PAS transcription factor. We have performed a set of microarray experiments aimed at identifying genes that are differentially regulated by SIM2, and successfully verified that the Myomesin2 (Myom2) gene is SIM2-responsive. Although SIM2 has been reported to be a transcription repressor, we find that SIM2 induces transcription of Myom2 and activates the Myom2 promoter sequence when co-expressed with the heterodimeric partner protein, ARNT1, in human embryonic kidney cells. Truncation and mutation of the Myom2 promoter sequence, combined with chromatin immunoprecipitation studies in cells, has lead to the delineation of a non-canonical E-box sequence 5'-AACGTG-3' that is bound by SIM2/ARNT1 heterodimers. Interestingly, in immortalized human myoblasts knock down of Sim2 results in increased levels of Myom2 RNA, suggesting that SIM2 is acting as a repressor in these cells and so its activity is likely to be highly context dependent. This is the first report of a direct SIM2/ARNT1 target gene with accompanying analysis of a functional response element.
Neurons display a myriad of dendritic architectures, reflecting their diverse roles in information processing and transduction in the nervous system. Recent findings suggest that neuronal signals may ...not account for all aspects of dendrite morphogenesis. Observations from C. elegans and other organisms suggest that glial cells can affect dendrite length and guidance, as well as localization and shapes of dendritic receptive structures, such as dendritic spines and sensory cilia. Thus, besides direct roles in controlling neuronal activity, glia contribute to neuron function by ensuring that neurons attain their proper shapes.
Some of the most spectacular examples of botanical carnivory—in which predator plants catch and digest animals presumably to supplement the nutrient-poor soils in which they grow—occur within the ...Droseraceae family. For example, sundews of the genus
Drosera
have evolved leaf movements and enzyme secretion to facilitate prey digestion. The molecular underpinnings of this behavior remain largely unknown; however, evidence suggests that prey-induced electrical impulses are correlated with movement and production of the defense hormone jasmonic acid (JA), which may alter gene expression. In noncarnivorous plants, JA is linked to electrical activity via changes in cytoplasmic Ca
2+
. Here, we find that dynamic Ca
2+
changes also occur in sundew (
Drosera spatulata
) leaves responding to prey-associated mechanical and chemical stimuli. Furthermore, inhibition of these Ca
2+
changes reduced expression of JA target genes and leaf movements following chemical feeding. Our results are consistent with the presence of a conserved Ca
2+
-dependent JA signaling pathway in the sundew feeding response and provide further credence to the defensive origin of plant carnivory.
PDF
